Intracellular Ca2+ and antioxidant values induced positive effect on fertilisation ratio and oocyte quality of granulosa cells in patients undergoing in vitro fertilisation
Esra Nur Tola A , Muhittin Tamer Mungan A , Abdülhadi Cihangir Uğuz B and Mustafa Nazıroğlu B CA Department of Obstetrics and Gynaecology, Faculty of Medicine, Suleyman Demirel University, TR-32260, Isparta, Turkey.
B Department of Biophysics, Faculty of Medicine, Suleyman Demirel University, TR-32260, Isparta, Turkey.
C Corresponding author. Email: mnaziroglu@med.sdu.edu.tr
Reproduction, Fertility and Development 25(5) 746-752 https://doi.org/10.1071/RD12144
Submitted: 12 March 2012 Accepted: 19 June 2012 Published: 2 August 2012
Abstract
Oxidative stress is important for promoting oocyte maturation and ovulation within the follicle through calcium ion (Ca2+) influx. The relationship between antioxidant and cytosolic Ca2+ levels and oocyte quality and fertilisation rate in the granulosa cells of patients undergoing in vitro fertilisation was investigated. Granulosa cells were collected from 33 patients. Cytosolic free Ca2+ ([Ca2+]i) concentration, lipid peroxidation, reduced glutathione, glutathione peroxidase and oocyte quality were measured in the granulosa cells. The relationship between two drug protocols was also examined (gonadotrophin-releasing hormone antagonist and agonist protocols) and the same parameters investigated. The [Ca2+]i concentration (P < 0.001), glutathione (P < 0.05) and oocyte quality (P < 0.001) values were significantly higher in the fertilised group than in the non-fertilised group, although glutathione peroxidase activity was significantly (P < 0.05) higher in the non-fertilised group than in the fertilised group. The [Ca2+]i concentrations were also higher (P < 0.001) in the good-quality oocyte groups than in the poor-quality oocyte group. There was no correlation between the two drug protocols and investigated parameters. In conclusion, it was observed that high glutathione and cytosolic Ca2+ concentrations in granulosa cells of patients undergoing in vitro fertilisation tended to increase the fertilisation potential of oocytes.
Additional keywords: antioxidant, Ca2+ signalling, oxidative stress.
References
Agarwal, A., Gupta, S., and Sikka, S. (2006). The role of free radicals and antioxidants in reproduction. Curr. Opin. Obstet. Gynecol. 18, 325–332.| The role of free radicals and antioxidants in reproduction.Crossref | GoogleScholarGoogle Scholar | 16735834PubMed |
Aguirre, P., Mena, N., Tapia, V., Rojas, A., Arredondo, M., and Núñez, M. T. (2006). Antioxidant responses of cortex neurons to iron loading. Biol. Res. 39, 103–104.
| Antioxidant responses of cortex neurons to iron loading.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVeqtbc%3D&md5=224a62f74bcb99d11dcd6e31d4decee9CAS | 16629170PubMed |
Ceylan, B. G., Nazıroğlu, M., Uğuz, A. C., Barak, C., Erdem, B., and Yavuz, L. (2011). Effects of vitamin C and E combination on element and oxidative stress levels in the blood of operative patients under desflurane anaesthesia. Biol. Trace Elem. Res. 141, 16–25.
| Effects of vitamin C and E combination on element and oxidative stress levels in the blood of operative patients under desflurane anaesthesia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1Gms7g%3D&md5=2029bf8d5402786b1e6fefb9528f4276CAS | 20464539PubMed |
Csordás, G., and Hajnoczky, G. (2009). SR/ER-mitochondrial local communication: calcium and ROS. Biochim. Biophys. Acta 1787, 1352–1362.
| SR/ER-mitochondrial local communication: calcium and ROS.Crossref | GoogleScholarGoogle Scholar | 19527680PubMed |
Das, S., Chattopadhyay, R., Ghosh, S., Ghosh, S., Goswami, S. K., Chakravarty, B. N., and Chaudhury, K. (2006). Reactive oxygen species level in follicular fluid – embryo quality marker in IVF? Hum. Reprod. 21, 2403–2407.
| Reactive oxygen species level in follicular fluid – embryo quality marker in IVF?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVWlt7rK&md5=7b29b61b550730770b8e1400bc109578CAS | 16861701PubMed |
Eisenbach, M. (1999). Sperm chemotaxis. Rev. Reprod. 4, 56–66.
| Sperm chemotaxis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtVeht7c%3D&md5=f927cfef3c374ecb2ed2ad7c0887d25cCAS | 10051103PubMed |
El Mouatassim, S., Guerin, P., and Menezo, Y. (1999). Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol. Hum. Reprod. 5, 720–725.
| Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1Mzlt1Cnsg%3D%3D&md5=afeddf31c038269e1af739b0741df800CAS | 10421798PubMed |
Galione, A. (1994). Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling. Mol. Cell. Endocrinol. 98, 125–131.
| Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsF2iur0%3D&md5=7aa5178616ade9036e659144e52c1d4eCAS | 8143921PubMed |
Galione, A., Lee, H. C., and Busa, W. B. (1991). Ca(2+)-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143–1146.
| Ca(2+)-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt1yrtr8%3D&md5=18344b0dad4289de59f822c368c45b26CAS | 1909457PubMed |
Galione, A., Cui, Y., Empson, R., Iino, S., Wilson, H., and Terrar, D. (1998). Cyclic ADP-ribose and the regulation of calcium-induced calcium release in eggs and cardiac myocytes. Cell Biochem. Biophys. 28, 19–30.
| Cyclic ADP-ribose and the regulation of calcium-induced calcium release in eggs and cardiac myocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns1yhsbk%3D&md5=152df3eb576ee64a27c8bad1c85c090dCAS | 9386890PubMed |
Gonzalez, F., Rote, N. S., Minium, J., and Kirwan, J. P. (2006). Reactive oxygen species-induced oxidative stress in the development of insulin resistance and hyperandrogenism in polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 91, 336–340.
| Reactive oxygen species-induced oxidative stress in the development of insulin resistance and hyperandrogenism in polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1aluw%3D%3D&md5=3ab79808888d04b5c388c64838e607dfCAS | 16249279PubMed |
Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440–3450.
| 1:CAS:528:DyaL2MXitVSmu7s%3D&md5=386efd8d651d4846939ade9d1d4ca9b1CAS | 3838314PubMed |
Heemskerk, J. W., Feijge, M. A., Henneman, L., Rosing, J., and Hemker, H. C. (1997). The Ca2+-mobilizing potency of alpha-thrombin and thrombin receptor-activating peptide on human platelets – concentration and time effects of thrombin-induced Ca2+ signalling. Eur. J. Biochem. 249, 547–555.
| The Ca2+-mobilizing potency of alpha-thrombin and thrombin receptor-activating peptide on human platelets – concentration and time effects of thrombin-induced Ca2+ signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFelsbc%3D&md5=e7a80a7d6d9ac2076f25f5a4a2dbc904CAS | 9370366PubMed |
Jaffe, L. A., and Cross, N. L. (1986). Electrical regulation of sperm–egg fusion. Annu. Rev. Physiol. 48, 191–200.
| Electrical regulation of sperm–egg fusion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283htlykuw%3D%3D&md5=44d1fce8dd15a4763164ae594b182ccaCAS | 2423022PubMed |
Jančar, N., Kopitar, A. N., Ihan, A., Virant Klun, I., and Bokal, E. V. (2007). Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilisation and blastocyst development. J. Assist. Reprod. Genet. 24, 91–97.
| Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilisation and blastocyst development.Crossref | GoogleScholarGoogle Scholar | 17216562PubMed |
Lawrence, R. A., and Burk, R. F. (1976). Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71, 952–958.
| Glutathione peroxidase activity in selenium-deficient rat liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlsVWls7s%3D&md5=397aaf6e53b5a7fd220b2a5065eb3c28CAS | 971321PubMed |
Lee, K. S., Joo, B. S., Na, Y. J., Yoon, M. S., Choi, O. H., and Kim, W. W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–498.
| Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrmsVKisQ%3D%3D&md5=969337f653ab867a22bd08d4aaefa816CAS | 11665664PubMed |
Lerner, I., Trus, M., Cohen, R., Yizhar, O., Nussinovitch, I., and Atlas, D. (2006). Ion interaction at the pore of Lc-type Ca2+ channel is sufficient to mediate depolarization-induced exocytosis. J. Neurochem. 97, 116–127.
| 1:CAS:528:DC%2BD28XjslarsL4%3D&md5=a48426f427ed0b5a75eca0e04f92ede7CAS | 16515555PubMed |
Livneh, A., Cohen, R., and Atlas, D. (2006). A novel molecular inactivation determinant of voltage-gated CaV1.2 L-type Ca2+ channel. Neuroscience 139, 1275–1287.
| A novel molecular inactivation determinant of voltage-gated CaV1.2 L-type Ca2+ channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVGhurc%3D&md5=b33ab85a9a97b38128e822369c5b7ce7CAS | 16533566PubMed |
Lowry, O. H., Rosenbrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
| 1:CAS:528:DyaG38XhsVyrsw%3D%3D&md5=bec303a88518a087fe23019c55fbf632CAS | 14907713PubMed |
Matos, L., Stevenson, D., Gomes, F., Silva-Carvalho, J. L., and Almeida, H. (2009). Superoxide dismutase expression in human cumulus oophorus cells. Mol. Hum. Reprod. 15, 411–419.
| Superoxide dismutase expression in human cumulus oophorus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslKjs78%3D&md5=6182afce87518f60bb6e296ef888bcc0CAS | 19482907PubMed |
McDougall, A., Shearer, J., and Whitaker, M. (2000). The initiation and propagation of the fertilisation wave in sea urchin eggs. Biol. Cell 92, 205–214.
| The initiation and propagation of the fertilisation wave in sea urchin eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslegs7Y%3D&md5=b64d4247ef7b7c1b738dab3217ab0a85CAS | 11043409PubMed |
McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P., and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilisation and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
| Human cumulus granulosa cell gene expression: a predictor of fertilisation and embryo selection in women undergoing IVF.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crotVyisA%3D%3D&md5=4c220a7324f72551a6aa60a07142b155CAS | 15471935PubMed |
Miyazaki, S., Yuzaki, M., Nakada, K., Shirakawa, H., Nakanishi, S., Nakade, S., and Mikoshiba, K. (1992). Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilised hamster eggs. Science 257, 251–255.
| Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilised hamster eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVyrurg%3D&md5=9705181f59b9bd1b6c9b8544b4f94fc5CAS | 1321497PubMed |
Miyazaki, S., Shirakawa, H., Nakada, K., and Honda, Y. (1993). Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilisation of mammalian eggs. Dev. Biol. 158, 62–78.
| Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilisation of mammalian eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFCjsL0%3D&md5=e0f6b044a99d9a3fbc00f321fd928b4dCAS | 8392472PubMed |
Nazıroğlu, M. (2007). New molecular mechanisms on the activation of TRPM2 channels by oxidative stress and ADP-ribose. Neurochem. Res. 32, 1990–2001.
| New molecular mechanisms on the activation of TRPM2 channels by oxidative stress and ADP-ribose.Crossref | GoogleScholarGoogle Scholar | 17562166PubMed |
Nazıroğlu, M. (2009). Role of selenium on calcium signalling and oxidative stress-induced molecular pathways in epilepsy. Neurochem. Res. 34, 2181–2191.
| Role of selenium on calcium signalling and oxidative stress-induced molecular pathways in epilepsy.Crossref | GoogleScholarGoogle Scholar | 19513830PubMed |
Nazıroğlu, M. (2011). TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem. Res. 36, 355–366.
| TRPM2 cation channels, oxidative stress and neurological diseases: where are we now?Crossref | GoogleScholarGoogle Scholar | 21140288PubMed |
Nazıroğlu, M., Özgül, M., Çiğ, B., Doğan, S., and Uğuz, A. C. (2011). Glutathione and 2-aminoethoxydiphenyl borate modulate Ca2+ influx and oxidative stress through TRPM2 channel in rat dorsal root ganglion neurons. J. Membr. Biol. 242, 109–118.
| Glutathione and 2-aminoethoxydiphenyl borate modulate Ca2+ influx and oxidative stress through TRPM2 channel in rat dorsal root ganglion neurons.Crossref | GoogleScholarGoogle Scholar | 21748272PubMed |
Özgül, C., and Nazıroğlu, M. (2012). TRPM2 channel protective properties of N-acetylcysteine on cytosolic glutathione depletion dependent oxidative stress and Ca2+ influx in rat dorsal root ganglion. Physiol. Behav. 106, 122–128.
| TRPM2 channel protective properties of N-acetylcysteine on cytosolic glutathione depletion dependent oxidative stress and Ca2+ influx in rat dorsal root ganglion.Crossref | GoogleScholarGoogle Scholar | 22300897PubMed |
Özkaya, M. O., and Nazıroğlu, M. (2010). Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilisation. Fertil. Steril. 94, 2465–2466.
| Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilisation.Crossref | GoogleScholarGoogle Scholar | 20226443PubMed |
Pasqualotto, E. B., Agarwal, A., Sharma, R. K., Izzo, V. M., Pinotti, J. A., Joshi, N. J., and Rose, B. I. (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil. Steril. 81, 973–976.
| Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFCrtrc%3D&md5=b93fda3b61f2f11e700f6541acb21b5eCAS | 15066450PubMed |
Paszkowski, T., and Clarke, R. N. (1996). Antioxidative capacity of preimplantation embryo culture medium declines following the incubation of poor-quality embryos. Hum. Reprod. 11, 2493–2495.
| Antioxidative capacity of preimplantation embryo culture medium declines following the incubation of poor-quality embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7jsFKjtw%3D%3D&md5=178c8f2f32a37c99e5675d7e984839e9CAS | 8981142PubMed |
Placer, Z. A., Cushman, L. L., and Johnson, B. C. (1966). Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal. Biochem. 16, 359–364.
| Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XksFymsLs%3D&md5=c887966a48832d32a151ed7b64fe11c8CAS | 6007581PubMed |
Sedlak, J., and Lindsay, R. H. (1968). Estimation of total, protein-bound and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem. 25, 192–205.
| Estimation of total, protein-bound and nonprotein sulfhydryl groups in tissue with Ellman’s reagent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXhslCktA%3D%3D&md5=ecf55ab15a68d0523106abb93c8413bfCAS | 4973948PubMed |
Seino, T., Saito, H., Kaneko, T., Takahashi, T., Kawachiya, S., and Kurachi, H. (2002). Eight-hydroxy-2’-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilisation–embryo transfer program. Fertil. Steril. 77, 1184–1190.
| Eight-hydroxy-2’-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilisation–embryo transfer program.Crossref | GoogleScholarGoogle Scholar | 12057726PubMed |
Silvestre, F., Boni, R., Fissore, R. A., and Tosti, E. (2011). Ca2+ signalling during maturation of cumulus–oocyte complex in mammals. Mol. Reprod. Dev. 78, 744–756.
| Ca2+ signalling during maturation of cumulus–oocyte complex in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7vJ&md5=ea0191a0dfd5c53e15249c13f6804babCAS | 21656870PubMed |
Steinhardt, R. A., Lundin, L., and Mazia, D. (1971). Bioelectric responses of the echinoderm egg to fertilisation. Proc. Natl. Acad. Sci. USA 68, 2426–2430.
| Bioelectric responses of the echinoderm egg to fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XmvFKnsw%3D%3D&md5=45b90161834c46cd239f5fd3c9df5822CAS | 5289876PubMed |
Tamura, H., Takasaki, A., Miwa, I., Taniguchi, K., Maekawa, R., Asada, H., Taketani, T., Matsuoka, A., Yamagata, Y., Shimamura, K., Morioka, H., Ishikawa, H., Reiter, R. J., and Sugino, N. (2008). Oxidative stress impairs oocyte quality and melatonin protects oocytes from free-radical damage and improves fertilisation rate. J. Pineal Res. 44, 280–287.
| Oxidative stress impairs oocyte quality and melatonin protects oocytes from free-radical damage and improves fertilisation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1ansLk%3D&md5=d3288c7bc14f1288c576bfac1d169b08CAS | 18339123PubMed |
Tatemoto, H., Sakurai, N., and Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805–810.
| Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCiu78%3D&md5=94405b7a063834d36079657031e3d253CAS | 10952924PubMed |
Uğuz, A. C., Nazıroğlu, M., Espino, J., Bejarano, I., Gonzalez, D., Rodriguez, A. B., and Pariente, J. A. (2009). Selenium modulates oxidative stress-induced cell apoptosis in human myeloid HL-60 cells through regulation of calcium release and caspase-3 and -9 activities. J. Membr. Biol. 232, 15–23.
| Selenium modulates oxidative stress-induced cell apoptosis in human myeloid HL-60 cells through regulation of calcium release and caspase-3 and -9 activities.Crossref | GoogleScholarGoogle Scholar | 19898892PubMed |
Van Soom, A., Tanghe, S., De Pauw, I., Maes, D., and de Kruif, A. (2002). Function of the cumulus oophorus before and during mammalian fertilisation. Reprod. Domest. Anim. 37, 144–151.
| Function of the cumulus oophorus before and during mammalian fertilisation.Crossref | GoogleScholarGoogle Scholar | 12071888PubMed |
Wang, Y., Sharma, R. K., Falcone, T., Goldberg, J., and Agarwal, A. (1997). Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil. Steril. 68, 826–830.
| Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c%2FltFanuw%3D%3D&md5=3f3772ce575a22a1f08d510291b8e4a5CAS | 9389810PubMed |
Wilding, M., Di Matteo, L., D’Andretti, S., Montanaro, N., Capobianco, C., and Dale, B. (2007). An oocyte score for use in assisted reproduction. J. Assist. Reprod. Genet. 24, 350–358.
| An oocyte score for use in assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 17629723PubMed |
Yang, H. W., Hwang, K. J., Kwon, H. C., Kim, H. S., Choi, K. W., and Oh, K. S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod. 13, 998–1002.
| Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjs12gurs%3D&md5=b593d4213b1b345a7f7ea7a612d0d495CAS | 9619561PubMed |